Psychobiological Roots of Early

Attachment
Myron A. Hofer
Sackler Institute for Developmental Psychobiology and Department of Psychiatry, Columbia University College
of Physicians & Surgeons
ABSTRACTNew laboratory research has revealed a net-
work of simple behavioral, physiological, and neural
processes that underlie the psychological constructs of at-
tachment theory. It has become apparent that the unique
features of early infant attachment reect certain unique
features of early infant sensory and motor integration,
learning, communication, and motivation, as well as the
regulation of biobehavioral systems by the motherinfant
interaction. In this article, I will use this new knowledge to
answer three major questions that have remained unset-
tled in our understanding of early human attachment:
What creates an attachment bond? Why is early maternal
separation stressful? How can early relationships have
lasting effects? I will discuss the implications of these new
answers for human infants and for the development of
mental processes. Attachment remains useful as a concept
that, like hunger, describes the operation of subprocesses
that work together within the frame of a vital biological
function.
KEYWORDSattachment; separation; bond; maternal be-
havior; early experience; learning
The word attachment has assumed newmeanings as it has spread
fromliterature to psychology, and most recently to biology. These
changes have spanned the half century since the Second World
War, when the vast numbers of displaced and orphaned children
made the importance of a childs early tie to its mother evident to
all. As different groups within psychology used the concept,
there developed champions and detractors of one or another
formulation. I think that a crucial change came when Bowlbys
(1982) concept of attachment as a unique motivational system
was gradually found to be incapable of generating testable
hypotheses that could explain several puzzling observations.
Developmental psychobiology researchers focused instead on
simpler processes at work within the interactions between infant
and parentsuch as orientation, nursing, early learning,
thermoregulation, and sensorimotor-systemdevelopment. There
was a period between the early 1970s and late 1980s when at-
tachment was seldom used by developmental psychobiologists.
In the last decade, however, the word has found a newusefulness
as a general descriptive termfor the processes that maintain and
regulate sustained social relationships, much the same way that
appetite refers to a cluster of behavioral and physiological
processes that regulate food intake.
The concept of attachment provides a good example of how a
psychological construct can be analyzed at the level of the
component processes that underlie it. This approach does not
attempt to reduce psychological questions to the most basic units
of biological organization. Rather, the focus is on the processes
of behavioral and physiological regulation that closely underlie
psychological constructs, providing a much-needed link be-
tween psychology and the cellular/molecular mechanisms of
brain function. New knowledge at the level of behavior and in-
tegrative physiology promises to deepen our understanding of
psychological constructs rather than eliminate the need for
them.
In order to illustrate this point, I will describe how new re-
search using animal models has helped resolve three questions
left unanswered by psychological theories of attachment, and I
will relate these ndings to human psychology, as I see it.
WHAT CREATES AN ATTACHMENT BOND?
This question asks what processes are responsible for the de-
velopment of the behaviors, and inferred mental states, that we
refer to as the bond between infant and mother. Research has
shown that predispositions can be created prenatally, in the fe-
tus, to respond preferentially to specific maternal scents and
sounds, and that these predispositions prepare the way for the
next phase in the development of attachment.
Address Correspondence to Myron A. Hofer, MD, Professor and Di-
rector, The Sackler Institute for Developmental Psychobiology, Co-
lumbia University College of Physicians and Surgeons, New York
State Psychiatric Institute, 1051 Riverside Drive, Unit #40, New
York, NY 10032; e-mail: mah6@columbia.edu.
CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE
84 Volume 15Number 2 Copyright r2006 Association for Psychological Science
Regina Sullivan, Steve Brake, and I (Sullivan, Hofer, &Brake,
1986) discovered an experimental learning paradigm in new-
born rats that revealed a rapid and powerful learning capacity by
which neonates acquire the ability to discriminate, prefer, ap-
proach, and maintain proximity to their own mother. A specific
neutral odor was presented to newborns while the pups were
stroked with an artists brush for 5 to 15 minutes. The odor was
later applied to shavings under mesh in a two-compartment box.
The neonates then turned preferentially to that odor and re-
mained on the mesh over the scented compartment for the du-
ration of testing. Control subjects were presented with the same
stimuli but separated in time. They showed no later preference
for the odor. Such rapid and specific associative learning had not
been anticipated in rats of such an early age. Indeed Bowlby and
others in the 1960s thought that even human newborns and
young infants interacted with their mothers entirely through
reex and xed-action-pattern behaviors (simple, rigidly stere-
otyped action sequences). We now know that human newborns
also can distinguish their own mothers smell, apparently on the
basis of prenatal experience, and add vocal and visual recog-
nition postnatallyprobably by similar early-learning systems
(Winberg 2005).
Next, Sullivan (reviewed in Moriceau and Sullivan, 2005)
discovered that for the rst 10 days after birth, an aversive level
of stimulation (e.g., tail pinch, mild shock) that itself elicits
vigorous escape behavior will paradoxically induce approach
and preference for an odor previously associated with it. After
those 10 days, such associative pairing results in avoidance of
the odor. The unexpected early aversive-preference learning has
an obvious parallel in the strong attachments frequently ob-
served in abused human infants. In this animal model, Sullivan
and coworkers have mapped out the critical period for the effect,
have shown that the critical period can be extended in time by
daily repetitions of the associative experience, and have related
the normal close of this period to developmental transitions in
specific brain systems that are regulated by circulating adreno-
cortical hormones.
In these studies, the questions of the nature of a psychological
bond, its specicity, and how it is formed, can be answered in
terms of an unexpected rapid early-learning process with
properties that can be related to brain and hormone-system
development. Experiments testing alternative hypotheses led us
to a new way to understand the paradoxically close attachments
of children to abusive parents.
WHY IS EARLY MATERNAL SEPARATION STRESSFUL?
In most conceptual formulations of attachment, the separation
response is explained as deriving from the strong affective na-
ture of the bond, which when severed or ruptured by separa-
tion results in a series of traumatic emotional reactions: the
biphasic protestdespair response, in which an initial burst of
calling and active search behavior is followed by a long decline
in behavioral responsiveness (Bowlby, 1982; see Fig. 1). But
there is circularity in this line of reasoning, as the evidence for
the existence of the bond itself, and for its strength, lies in the
dramatic response to its being broken by separation.
I was led to an entirely different way of thinking about sepa-
ration by unexpected results in our laboratory (reviewed in
Hofer, 1994). Initially, we did not believe that infant rats were
capable of the complex cognitive-affective processes thought to
underlie the separation response seen in infant monkeys and
humans. But to our surprise, we found that, like primate infants,
infant rats show a complex biphasic protestdespair response to
maternal separation, as well as a number of other responses that
were entirely unexpected. We found that these changes were not
the expression of an integrated psychophysiological response
(like the increase in heart rate and respiration during exercise) to
the stressful event, but were the result of a novel mechanism I
will nowdescribe (see Fig. 2). Our experiments showed that each
of the individual behavioral and physiological systems of the
infant rat was responding to the loss of one or another of the
components (e.g., nutrient, thermal/metabolic, or sensorimotor)
of the infants previous interaction with its mother and that the
complex response to separation was due to the withdrawal of all
these components at once.
For example, we found that providing one of these compo-
nents, warmth, to a separated pup prevented the slow decline in
Fig. 1. Schematic representation of the dynamics of early-separation
responses based on the concept of an attachment bond as described by
John Bowlby (Bowlby, 1982).
Fig. 2. Schematic representation of the dynamics of early-separation
responses resulting from the loss of regulatory interactions within the
motherinfant relationship.
Volume 15Number 2 85
Myron A. Hofer
the pups general activity level (a response similar to Bowlbys
despair phase), but this had no effect on responses in other
systems. The pups cardiac rate continued to fall by 40%, re-
gardless of whether supplemental heat or tactile stimulation was
provided. But we found that we could maintain cardiac rate in
separated pups at normal levels by continuous infusion of milk to
the pups stomach. Supplying enough milk to prevent weight loss
had no effect, but if enough was given to produce a normal range
of weight gain, the cardiac rate at the end of a 24-hour separation
was proportional to the amount of nutrient that had been infused.
In other words, the supplied milk regulated the pups heart rate.
The physiological mechanism, we found, was not gastric dis-
tention or any effect of absorbed nutrients, but an effect of
specific nutrients on receptors in the lining of the stomach that
are connected to the brain.
We concluded from these surprising results that warmth pro-
vided by the mother normally maintained the pups activity level
and that her milk maintained her pups heart rate. Maternal
separation withdrew these regulatory inuences that were hid-
den within the ordinary motherinfant interactions, resulting in
slowed behavior and low heart rate. We began to look for other
effects of separation and the specific regulators that could pre-
vent them. We found that sufcient levels of tactile stimulation
during a 24-hour separation period prevented the increase in the
pups behavioral response to being moved into a novel test
chamber, a behavioral hyper-reactivity that we had found in
separated pups with normal body temperatures. Graded levels of
tactile stimulation during separation produced graded levels of
quieting of pups. For the rate of sucking on an articial teat and
for the immediate vocal protest phase of vocalization (Hofer,
1996), both of which increased in separated pups, more specific
types of sensorimotor experience were necessary to reduce these
behaviors to normal levels. We also studied sleep/wake states
using an electroencephalograph and found that the durations of
bouts of sleeping and waking and the smooth transitions between
themwere maintained (regulated) by the periodicity or rhythmof
maternal milk supply and tactile interactions, rather than simply
by their level. After 24 hours of separation, the REM-sleep time
of pups remaining in their home cage was sharply decreased and
slow-wave sleep was fragmented by frequent short awakenings.
Only scheduled periodic bouts of nutrient infusion and tactile
stimulation prevented this. Soon, other investigators were able to
dene other maternal regulatory effects: Saul Schanberg for
growth hormone and Seymour Levine for adrenocortical system
control (reviewed in Hofer, 1994).
In thinking about the implication of these ndings for human
infants, one can suppose that these kinds of simple maternal
regulators would be found early in a babys postnatal period, but
that soon more subtle and intricate interactions would become
important. Reciprocity, imitation, attunement, and play are now
being investigated for their roles in regulating the babys affec-
tive state and his or her developing capacity to self-regulate and
later engage in complex social interactions outside the parental
relationship. But we should be aware that regulatory interactions
at the simpler levels of touch, warmth, and smell may continue to
be important for humans (as well as other animals), even into
adult life, with implications for human grief (Hofer, 1984).
In trying to understand responses to separation in infants (as
well as in adults), we should look carefully for exactly what was
lost, not simply regard separation as an affective response to
stress. The discovery of numerous regulatory processes hidden
within the motherinfant interaction provides a novel causative
explanation for the response of infants to maternal separation
that does not depend upon the metaphorical concept of a bond
that is broken. Furthermore, the discovery of these regulatory
processes at work within an ongoing motherinfant relationship
raises the question of whether, in addition, they might be re-
sponsible for regulating the course of development over time.
HOWCAN EARLY RELATIONSHIPS HAVE LASTING
EFFECTS?
An immediate implication of our discovery of multiple hidden
regulators within the motherinfant interaction was the possi-
bility that different patterns of early parentinfant interaction
might differentially shape the course of development of off-
spring. The rst pattern that we investigated was the early ter-
mination of the relationship, before the usual time of weaning
(reviewed in Hofer, 1994). We found that if rat pups are
separated from their mothers at 15 days instead of the usual
21 to 30 days, they can survive, but they will have been
deprived of maternal regulation during that period of their
development. We assessed the effect of this early weaning on the
vulnerability of adults to a known stressor, 24 hours of immo-
bilization, which had been reported to produce gastric ulceration
in about 50% of normally reared adult rats. We found that early
weaning did not affect the expected percent vulnerability when
rats were stressed in adulthood (120 days); but in early adoles-
cence (25 and 35 days), 80%of the early-weaned rats developed
ulcers, and these were larger and deeper than those occurring
in adults; however, no normally reared rats developed ulcers at
these ages. In the immediate aftermath of maternal separation,
at 17 days of age, no rat ulcerated. Even more surprising, as
rats matured into later adulthood (160 days), the early-weaned
rats were actually less vulnerable than the normally reared
ones were.
What I believe this experiment illustrates is that when all
maternal regulators are withdrawn early, a number of physio-
logical and behavioral systems are altered in their develop-
mental paths and in their relation to each other, creating a
complex, changing pattern of vulnerability over the life span.
We then decided to study a more discrete formof change in the
pattern of early motherinfant interactions by taking advantage
of naturally occurring variations in the relative frequency of
different maternal behaviors, what might be called different
qualities of the relationship. Michael Myers, Harry Shair, and
86 Volume 15Number 2
Psychobiological Roots of Early Attachment
I (Myers, Shair, & Hofer, 1992) were studying two strains of rats
created by selective breeding, the spontaneously hypertensive
strain and the normotensive-progenitor strain. We found a range
of variation between litters in their mean adult blood pressure.
We then observed a range of variation in the levels of 10 different
maternal behaviors as we studied litters over the preweaning
period. Within each strain, the offspring of mothers with high
levels of three of these behaviors (licking-grooming, high-arched
nursing posture, and time in contact) had significantly higher
levels of blood pressure as adults than did offspring of mothers
with low levels of those behaviors. (Since the animals in each
strain had been inbred to the point that they were genetically
identical, these differences could not be simply due to genetic
covariation in maternal behavior and in blood pressure within
each strain.) Furthermore, the mothers of the spontaneously
hypertensive strain, as a group, showed higher levels of these
maternal behaviors than did the mothers of the normotensive
strain.
Finding such a strong correlation of levels of specific maternal
behaviors with levels of offspring blood pressure in adulthood
strongly supported our inference that certain components of the
motherinfant interaction serve to regulate the later develop-
mental paths of certain systems in their offspring. Subsequent
research by Michael Meaney and his group, recently reviewed in
this journal (Parent et al., 2005), found that two of these same
behaviors (licking-grooming and high-arched nursing posture)
predicted levels of adult offspring responses in a wide variety of
other systems (e.g., adrenocortical and fear responses, cognitive
function, and even maternal behavior in the next generation).
Variations in qualities of motherinfant relationships among
humans thus appear to have deep biological roots in the form of
their capacity to shape childrens psychological and biological
responses to their environmenteffects that extend into adult-
hood.
LINKS TO HUMAN MENTAL PROCESSES
In applying these experimental results to early human devel-
opment, we can begin to see how the psychological constructs of
the attachment bond and the traumatic effects of maternal
separation originate, in one case, in an unusual form of rapid
early learning and, in the other, in the unexpected develop-
mental regulatory functions being carried out by specific
motherinfant interactions. These processes can be thought of as
underlying the psychological concepts that people have in-
vented to help think about complex behaviors and mental ex-
periences. In humans, the early-learning processes and the
many different regulating interactions that I have described
above are the rst experiences out of which mental representa-
tions and their associated affects arise. It seems likely that these
mental structures combine the infants newly developing ca-
pacities to remember and anticipate events and respond to
symbolic cues with traces of the earlier functions of the maternal
regulatory interactions, through processes similar to the func-
tional links involved in the associative conditioning of physio-
logical responses. Thus, the internal working model of
attachment theory is constructed as early biological regulatory
interactions become linked to later-developing memories, ex-
pectations, and affect states by the many associations of physical
and psychological events during this developmental transition
period between infancy and childhood, in the same way that the
salivation of Pavlovs dogs became linked to the expectation of
food through a series of prior associations. This may help explain
the visceral sensations accompanying the vicissitudes of close
human relationships even after the development of self-regula-
tion of affect and motivation come to supplant the sensorimotor,
thermal, and nutrient-based regulatory systems that are hidden
within the observable interactions of younger infants with their
mothers (Polan and Hofer, 1999).
The future directions of this research are, rst, to extend our
understanding of the actual links connecting specific mother
infant interactions (such as touch, voice, imitation) with devel-
oping psychological processes (on the one hand) and with cel-
lular/molecular brain processes via neural and hormonal
pathways (on the other); and, second, to nd out how these in-
teractions exert their effects on the developmental paths of be-
havior and biological systems, from infancy into adulthood.
Recommended Reading
Bowlby, J. (1982). (See References)
Cassidy, J., & Shaver, P.R. (Eds.). (1999). Handbook of attachment
theory and research. New York: Guilford Publications.
Hofer, M.A. (2002). The riddle of development. In D.J. Lewkowicz &R.
Lickliter (Eds.), Conceptions of Development (pp. 530) Philadel-
phia: Psychology Press.
Insel, T.R., & Fernald, R.D. (2004). How the brain processes social
information: Searching for the social brain. Annual Review of Ne-
uroscience, 27, 697722.
AcknowledgmentsThis work was supported by project grants
and a Research Scientist Award from the National Institutes of
Mental Health and by the Sackler Institute for Developmental
Psychobiology at Columbia University.
REFERENCES
Bowlby, J. (1982). Attachment (2nd ed.). New York: Basic Books.
Hofer, M.A. (1984). Relationships as regulators: A psychobiologic
perspective on bereavement. Psychosomatic Medicine, 46, 183
197.
Hofer, M.A. (1994). Early relationships as regulators of infant physi-
ology and behavior. Acta Paediatrica, 397(Suppl.), 918.
Hofer, M.A. (1996). Multiple regulators of ultrasonic vocalization in the
infant rat. Psychoneuroendocrinology, 21, 203217.
Moriceau, S., &Sullivan, R. (2005). Neurobiology of infant attachment.
Developmental Psychobiology, 47, 230246.
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Myron A. Hofer
Myers, M.M., Shair, H.N., & Hofer, M.A. (1992). Feeding in infancy:
Short- and long-term effects on cardiovascular function. Ex-
perientia, 48, 322333.
Parent, C., Zhang, T., Caldji, C., Bagot, R., Champagne, F., Pruessner,
J., &Meaney, M. (2005). Maternal care and individual differences
in defensive responses. Current Directions in Psychological Sci-
ence, 14, 229233.
Polan, H.J., & Hofer, M.A. (1999). Psychobiological origins of infant
attachment and separation responses. In J. Cassidy & P.R. Shaver
(Eds.), Handbook of attachment theory and research (pp. 162180).
New York: Guilford Publications.
Sullivan, R.M., Hofer, M.A., & Brake, S.C. (1986). Olfactory-guided
orientation in neonatal rats is enhanced by a conditional change in
behavior state. Developmental Psychobiology, 19, 615623.
Winberg, J. (2005). Mother and newborn baby: Mutual regulation of
physiology and behaviorA selective review. Developmental
Pychobiology, 47, 219229.
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